Plant Molecular Biology

, Volume 53, Issue 6, pp 805–820 | Cite as

Changes in gene expression in response to altered SHL transcript levels

  • Carsten MüssigEmail author
  • Thomas Altmann


The nuclear SHL protein is composed of a N-terminal BAH domain and a C-terminal PHD finger. Both domains are found in transcriptional regulators and chromatin-modifying proteins. Arabidopsis plants over-expressing SHL showed earlier flowering and senescence phenotype. To identify SHL regulated genes, expression profiles of 35S::SHL plants were established with Affymetrix ATH1 microarrays. About 130 genes showed reduced transcript levels, and about 45 genes showed increased transcript levels in 35S::SHL plants. The up-regulated genes included AGL20 and AGL9, which most likely cause the early flowering phenotype of 35S::SHL plants. Late-flowering SHL-antisense lines showed reduced AGL20 mRNA levels, suggesting that AGL20 gene expression depends on the SHL protein. The stronger expression of senescence- and defence-related genes (such as DIN2, DIN11 and PR-1) is in line with the early senescence phenotype of SHL-over-expressing plants. SHL-down-regulated genes included stress response genes and the PSR3.2 gene (encoding a β-glucosidase). SHL over-expression did not alter the tissue specificity of PSR3.2 gene expression, but resulted in reduced transcript levels in both shoots and roots. Plants with glucocorticoid-inducible SHL over-expression were established and used for expression profiling as well. A subset of genes was identified, which showed consistent changes in the inducible system and in plants with constitutive SHL over-expression.

Affymetrix BAH domain flowering time gene expression PHD finger senescence SHL 


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  1. Aasland, R., Gibson, T.J. and Stewart, A.F. 1995. The PHD finger: implications for chromatin-mediated transcriptional regulation. Trends Biochem. Sci. 20: 56–59.PubMedGoogle Scholar
  2. Adamson, A.L. and Shearn, A. 1996. Molecular genetic analysis of Drosophila ash2, a member of the trithorax group required for imaginal disc pattern formation. Genetics 144: 621–633.PubMedGoogle Scholar
  3. Amedeo, P., Habu, Y., Afsar, K., Mittelsten Scheid, O. and Paszkowski, J. 2000. Disruption of the plant gene MOM releases transcriptional silencing of methylated genes. Nature 405: 203–206.PubMedGoogle Scholar
  4. Anderson, M., Fair, K., Amero, S., Nelson, S., Harte, P.J. and Diaz, M.O. 2002. A new family of cyclophilins with an RNA recognition motif that interact with members of the trx/MLL protein family in Drosophila and human cells. Dev. Gen. Evol. 212: 107–113.Google Scholar
  5. Aoyama, T. and Chua, N.H. 1997. A glucocorticoid-mediated transcriptional induction system in transgenic plants. Plant J. 11: 605–612.PubMedGoogle Scholar
  6. Bartee, L., Malagnac, F. and Bender, J. 2001. Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Dev. 15: 1753–1758.PubMedGoogle Scholar
  7. Bell, S.P., Mitchell, J., Leber, J., Kobayashi, R. and Stillman, B. 1995. The multidomain structure of orc1p reveals similarity to regulators of DNA replication and transcriptional silencing. Cell 83: 563–568.PubMedGoogle Scholar
  8. Bochar, D.A., Savard, J., Wang, W.D., Lafleur, D.W., Moore, P., Cote, J. and Shiekhattar, R. 2000. A family of chromatin remodeling factors related to Williams syndrome transcription factor. Proc. Natl. Acad. Sci. USA 97: 1038–1043.PubMedGoogle Scholar
  9. Bordoli, L., Husser, S., Luthi, U., Netsch, M., Osmani, H. and Eckner, R. 2001. Functional analysis of the p300 acetyltransferase domain: the PHD finger of p300 but not of CBP is dispensable for enzymatic activity. Nucl. Acids Res. 29: 4462–4471.PubMedGoogle Scholar
  10. Borner, R., Kampmann, G., Chandler, J., Gleissner, R., Wisman, E., Apel, K. and Melzer, S. 2000. AMADS domain gene involved in the transition to flowering in Arabidopsis. Plant J. 24: 591–599.PubMedGoogle Scholar
  11. Cairns, B.R., Lorch, Y., Li, Y., Zhang, M.C., Lacomis, L., Erdjumentbromage, H., Tempst, P., Du, J., Laurent, B. and Kornberg, R.D. 1996. RSC, an essential, abundant chromatin-remodeling complex. Cell 87: 1249–1260.PubMedGoogle Scholar
  12. Callebaut, I., Courvalin, J.C. and Mornon, J.P. 1999 The BAH (bromo-adjacent homology) domain: a link between DNA methylation, replication and transcriptional regulation. FEBS Lett. 446: 189–193.PubMedGoogle Scholar
  13. Capili, A.D., Schultz, D.C., Rauscher, F.J. and Borden, K.L.B. 2001. Solution structure of the PHD domain from the KAP-1 corepressor: structural determinants for PHD, RING and LIM zinc-binding domains. EMBO J. 20: 165–177.PubMedGoogle Scholar
  14. Chamberlin, H.M. and Thomas, J.H. 2000. The bromodomain protein LIN-49 and trithorax-related protein LIN-59 affect development and gene expression in Caenorhabditis elegans. Development 127: 713–723.PubMedGoogle Scholar
  15. Eshed, Y., Baum, S.F. and Bowman, J.L. 1999. Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99: 199–209.PubMedGoogle Scholar
  16. Fujiki, Y., Yoshikawa, Y., Sato, T., Inada, N., Ito, M., Nishida, I. and Watanabe, A. 2001 Dark-inducible genes from Arabidopsis thaliana are associated with leaf senescence and repressed by sugars. Physiol. Plant. 111: 345–352.PubMedGoogle Scholar
  17. Fuks, F., Hurd, P.J., Deplus, R. and Kouzarides, T. 2003. The DNA methyltransferases associate with HP1 and the SUV39H1 histone methyltransferase. Nucl. Acids Res 31: 2305–2312.PubMedGoogle Scholar
  18. Gavin, K.A., Hidaka, M. and Stillman, B. 1995. Conserved initiator proteins in eukaryotes. Science 270: 1667–1671.PubMedGoogle Scholar
  19. Gibbons, R.J., McDowell, T.L., Raman, S., O'Rourke, D.M., Garrick, D., Ayyub, H. and Higgs, D.R. 2000. Mutations in ATRX, encoding a SWI/SNF-like protein, cause diverse changes in the pattern of DNA methylation. Nature Genet. 24: 368–371.PubMedGoogle Scholar
  20. Goodwin, G.H. and Nicolas, R.H. 2001. The BAH domain, polybromo and the RSC chromatin remodelling complex. Gene 268: 1–7.PubMedGoogle Scholar
  21. Halbach, T., Scheer, N. and Werr, W. 2000. Transcriptional activation by the PHD finger is inhibited through an adjacent leucine zipper that binds 14-3-3 proteins. Nucl. Acids Res. 28: 3542–3550.PubMedGoogle Scholar
  22. Henikoff, S. and Comai, L. 1998. A DNA methyltransferase homolog with a chromodomain exists in multiple polymorphic forms in Arabidopsis. Genetics 149: 307–318.PubMedGoogle Scholar
  23. Ito, T., Levenstein, M.E., Fyodorov, D.V., Kutach, A.K., Kobayashi, R. and Kadonaga, J.T. 1999. ACF consists of two subunits, Acf1 and ISWI, that function cooperatively in the ATP-dependent catalysis of chromatin assembly. Genes Dev. 13: 1529–1539.PubMedGoogle Scholar
  24. Jeddeloh, J.A., Stokes, T.L. and Richards, E.J. 1999. Maintenance of genomic methylation requires a SWI2/SNF2-like protein. Nature Genet. 22: 94–97.PubMedGoogle Scholar
  25. Kalkhoven, E., Teunissen, H., Houweling, A., Verrijzer, C.P. and Zantema, A. 2002. The PHD type zinc finger is an integral part of the CBP acetyltransferase domain. Mol. Cell Biol. 22: 1961–1970.PubMedGoogle Scholar
  26. Kang, H.G., Fang, Y.W. and Singh, K.B. 1999. A glucocorticoidinducible transcription system causes severe growth defects in Arabidopsis and induces defense-related genes. Plant J. 20: 127–133.PubMedGoogle Scholar
  27. Kehle, J., Beuchle, D., Treuheit, S., Christen, B., Kennison, J.A., Bienz, M. and Muller, J. 1998. dMi-2, a hunchback-interacting protein that functions in Polycomb repression. Science 282: 1897–1900.PubMedGoogle Scholar
  28. Le Douarin, B., You, J., Nielsen, A.L., Chambon, P. and Losson, R. 1998. TIF1α: a possible link between KRAB zinc finger proteins and nuclear repectors. J. Steroid Biochem. Mol. Biol. 65: 43–50.PubMedGoogle Scholar
  29. Linder, B., Newman, R., Jones, L.K., Debernardi, S., Young, B.D., Freemont, P., Verrijzer, C.P. and Saha, V. 2000. Biochemical analyses of the AF10 protein: the extended LAP/PHD-finger mediates oligomerisation. J. Mol. Biol. 299: 369–378.PubMedGoogle Scholar
  30. Lindroth, A.M., Cao, X.F., Jackson, J.P., Zilberman, D., McCallum, C.M., Henikoff S., and Jacobsen, S.E. 2001. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292: 2077–2080.PubMedGoogle Scholar
  31. Liu, Y.L., Oakeley, E.J., Sun, L.J. and Jost, J.P. 1998. Multiple domains are involved in the targeting of the mouse DNA methyltransferase to the DNA replication foci. Nucl. Acids Res. 26: 1038–1045.PubMedGoogle Scholar
  32. Lloyd, A.M., Schena, M., Walbot, V. and Davis, R.W. 1994. Epidermal cell fate determination in Arabidopsis: patterns defined by a steroid-inducible regulator. Science 266: 436–439.PubMedGoogle Scholar
  33. Malboobi, M.A. and Lefebvre, D.D. 1997. A phosphate-starvation inducible β-glucosidase gene (psr3.2) isolated from Arabidopsis thaliana is a member of a distinct subfamily of the BGA family. Plant Mol. Biol. 34: 57–68.PubMedGoogle Scholar
  34. Mandel, M.A. and Yanofsky, M.F. 1998. The Arabidopsis AGL9 MADS box gene is expressed in young flower primordia. Sex. Plant Reprod. 11: 22–28.Google Scholar
  35. Meehan, R.R. 2003. DNA methylation in animal development. Semin. Cell Dev. Biol. 14: 53–65.PubMedGoogle Scholar
  36. Müssig, C., Kauschmann, A., Clouse, S.D. and Altmann, T. 2000. The Arabidopsis PHD-finger protein SHL is required for proper development and fertility. Mol. Gen. Genet. 264: 363–370.PubMedGoogle Scholar
  37. Nicolas, R.H. and Goodwin, G.H. 1996. Molecular cloning of polybromo, a nuclear protein containing multiple domains including five bromodomains, a truncated HMG-box, and two repeats of a novel domain. Gene 175: 233–240.PubMedGoogle Scholar
  38. Nislow, C., Ray, E. and Pillus, L. 1997. SET1, a yeast member of the trithorax family, functions in transcriptional silencing and diverse cellular processes. Mol. Biol. Cell 8: 2421–2436.PubMedGoogle Scholar
  39. Nourani, A., Doyon, Y., Utley, R.T., Allard, S., Lane, W.S. and Cote, J. 2001. Role of an ING1 growth regulator in transcriptional activation and targeted histone acetylation by the NuA4 complex. Mol. Cell Biol. 21: 7629–7640.PubMedGoogle Scholar
  40. O'Connell, S., Wang, L.J., Robert, S., Jones, C.A., Saint, R. and Jones, R.S. 2001. Polycomb-like PHD fingers mediate conserved interaction with enhancer of zeste protein. J. Biol. Chem. 276: 43065–43073.PubMedGoogle Scholar
  41. Ogas, J., Kaufmann, S., Henderson, J. and Somerville, C. 1999. PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc. Natl. Acad. Sci. USA 96: 13839–13844.PubMedGoogle Scholar
  42. Papa, C.M., Springer, N.M., Muszynski, M.G., Meeley, R. and Kaeppler, S.M. 2001. Maize chromomethylase Zea methyltransferase2 is required for CpNpG methylation. Plant Cell 13: 1919–1928.PubMedGoogle Scholar
  43. Pelaz, S., Gustafson-Brown, C., Kohalmi, S.E., Crosby, W.L. and Yanofsky, M.F. 2001. APETALA1 and SEPALLATA3 interact to promote flower development. Plant J. 26: 385–394.PubMedGoogle Scholar
  44. Pijnappel, W., Schaft, D., Roguev, A., Shevchenko, A., Tekotte, H., Wilm, M., Rigaut, G., Seraphin, B., Aasland, R. and Stewart, A.F. 2001. The S. cerevisiae SET3 complex includes two histone deacetylases, Hos2 and Hst1, and is a meiotic-specific repressor of the sporulation gene program. Genes Dev. 15: 2991–3004.PubMedGoogle Scholar
  45. Quirino, B.F., Noh, Y.-S., Himelblau, E. and Amasino, R.M. 2000. Molecular aspects of leaf senescence. Trends Plant Sci. 5: 278–282.PubMedGoogle Scholar
  46. Saha, V., Chaplin, T., Gregorini, A., Ayton, P. and Young, B.D. 1995. The leukemia-associated-protein (LAP) domain, a cysteine-rich motif, is present in a wide range of proteins, including MLL, AF10, and MLLT6 proteins. Proc. Natl. Acad. Sci. USA 92: 9737–9741.PubMedGoogle Scholar
  47. Schultz, D.C., Friedman, J.R. and Rauscher, F.J. 2001. Targeting histone deacetylase complexes via KRAB-zinc finger proteins: the PHD and bromodomains of KAP-1 form a cooperative unit that recruits a novel isoform of the Mi-2α subunit of NuRD. Genes Dev. 15: 428–443.PubMedGoogle Scholar
  48. Sedkov, Y., Benes, J.J., Berger, J.R., Riker, K.M., Tillib, S., Jones, R.S. and Mazo, A. 1999. Molecular genetic analysis of the Drosophila trithorax-related gene which encodes a novel SET domain protein. Mech. Dev. 82: 171–179.PubMedGoogle Scholar
  49. Shamay, M., Barak, O. and Shaul, Y. 2002. HBXAP, a novel PHD-finger protein, possesses transcription repression activity. Genomics 79: 523–529.PubMedGoogle Scholar
  50. Skowyra, D., Zeremski, M., Neznanov, N., Li, M.Y., Choi, Y.M., Uesugi, M., Hauser, C.A., Gu, W., Gudkov, A.V. and Qin, J. 2001. Differential association of products of alternative transcripts of the candidate tumor suppressor ING1 with the mSin3/HDAC1 transcriptional corepressor complex. J. Biol. Chem. 276: 8734–8739.PubMedGoogle Scholar
  51. Speulman, E. and Salamini, F. 1995. A barley cDNA clone with homology to the DNA-binding domain of the steroid hormone receptors. Plant Sci. 106: 91–98.Google Scholar
  52. Tian, L and Chen, Z.J. 2001. Blocking histone deacetylation in Arabidopsis induces pleiotropic effects on plant gene regulation and development. Proc. Natl. Acad. Sci. USA 98: 200–205.PubMedGoogle Scholar
  53. Tripoulas, N.A., Hersperger, E., La Jeunesse, D. and Shearn, A. 1994. Molecular genetic analysis of the Drosophila melanogaster gene absent, small or homeotic discs1 (ash1). Genetics 137: 1027–1038.PubMedGoogle Scholar
  54. Tripoulas, N., Lajeunesse, D., Gildea, J. and Shearn, A. 1996. The Drosophila ash1 gene product, which is localized at specific sites on polytene chromosomes, contains a SET domain and a PHD finger. Genetics 143: 913–928.PubMedGoogle Scholar
  55. Wagner, D. and Meyerowitz, E.M. 2002. SPLAYED, a novel SWI/SNF ATPase homolog, controls reproductive development in Arabidopsis. Curr. Biol. 12: 85–94.PubMedGoogle Scholar
  56. Wu, K., Tian, L., Malik, K., Brown, D. and Miki, B. 2000. Functional analysis of HD2 histone deacetylase homologues in Arabidopsis thaliana. Plant J. 22: 19–27.PubMedGoogle Scholar
  57. Xue, Y.T., Canman, J.C., Lee, C.S., Nie, Z.Q., Yang, D.F., Moreno, G.T., Young, M.K., Salmon, E.D. and Wang, W.D. 2000. The human SWI/SNF-B chromatin-remodeling complex is related to yeast Rsc and localizes at kinetochores of mitotic chromosomes. Proc. Natl. Acad. Sci. USA 97: 13015–13020.PubMedGoogle Scholar
  58. Yochum, G.S. and Ayer, D.E. 2001. Pf1, a novel PHD zinc finger protein that links the TLE corepressor to the mSin3A-histone deacetylase complex. Mol. Cell Biol. 21: 4110–4118.PubMedGoogle Scholar
  59. Zhang, Z.G., Hayashi, M.K., Merkel, O., Stillman, B. and Xu, R.M. 2002. Structure and function of the BAH-containing domain of Orc1p in epigenetic silencing. EMBO J. 21: 4600–4611.PubMedGoogle Scholar
  60. Zhou, Y.G., Santoro, R. and Grummt, I. 2002. The chromatin remodeling complex NoRC targets HDAC1 to the ribosomal gene promoter and represses RNA polymerase I transcription. EMBO J. 21: 4632–4640.PubMedGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2003

Authors and Affiliations

  1. 1.Universität Potsdam – Genetik, c/o MPI für Molekulare Pflanzenphysiologie, Am Mühlenberg 1GolmGermany

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